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Published in: Clinical and Experimental Nephrology 6/2014

01-12-2014 | Original Article

Effect of a combined treatment with erythropoietin and melatonin on renal ischemia reperfusion injury in male rats

Authors: Nasser Ahmadiasl, Shokofeh Banaei, Alireza Alihemati, Behzad Baradaran, Ehsan Azimian

Published in: Clinical and Experimental Nephrology | Issue 6/2014

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Abstract

Background

Renal ischemia reperfusion (IR) is an important cause of renal dysfunction. It contributes to the development of acute renal failure. Oxidative damage from reactive oxygen species is considered to be the principal component involved in the pathophysiological tissue alterations observed during IR. The purpose of this study was to evaluate the effect of a combined treatment with erythropoietin (EPO) plus melatonin (MEL), which are known anti-inflammatory and antioxidant agents, in IR-induced renal injury in rats.

Methods

Wistar Albino rats were unilaterally nephrectomized and subjected to 45 min of renal pedicle occlusion followed by 24 h of reperfusion. MEL (10 mg/kg, i.p) and EPO (5000 U/kg, i.p) were administered prior to ischemia. After 24 h of reperfusion, blood samples were collected for the determination of superoxide dismutase (SOD), glutathione peroxidase (GPx), plasma levels of total antioxidant capacity (TAC), and malondialdehyde (MDA) and serum urea level. Also, renal samples were taken for histological evaluation.

Results

Ischemia reperfusion significantly increased urea, blood SOD, and GPx levels. Histological findings of the IR group indicated that there was increase in tubular and glomerular hyaline cast, thickening of Bowman capsule basement membrane, and renal impairment in the glomerular epithelium. Treatment with EPO and MEL significantly decreased blood SOD, GPx, and urea levels and increased TAC level. In the EPO + MEL group, while the histopathological changes were lower than those in EPO group, they were the same as MEL group.

Conclusion

EPO and MEL combination treatment exerted more nephroprotective effects than EPO treatment and nearly had protective effects similar to MEL treatment.
Literature
2.
go back to reference Anaya-Prado R, Toledo-Pereyra LH, Lentsch AB, Ward PA. Ischemia-reperfusion injury. J Surg Res. 2002;105:248–58.PubMedCrossRef Anaya-Prado R, Toledo-Pereyra LH, Lentsch AB, Ward PA. Ischemia-reperfusion injury. J Surg Res. 2002;105:248–58.PubMedCrossRef
3.
go back to reference Troppmann C, Gillingham KJ, Benedetti E, Almond PS, Gruessner RW, Najarian JS, Matas AJ. Delayed graft function, acute rejection, and outcome after cadaver renal transplantation: the multivariate analysis. Transplantation. 1995;59:962–8.PubMedCrossRef Troppmann C, Gillingham KJ, Benedetti E, Almond PS, Gruessner RW, Najarian JS, Matas AJ. Delayed graft function, acute rejection, and outcome after cadaver renal transplantation: the multivariate analysis. Transplantation. 1995;59:962–8.PubMedCrossRef
4.
go back to reference Masztalerz M, Wlodarczyk Z, Czuczejko J, Slupski M, Kedziora J. Superoxide anion as a marker of ischemia-reperfusion injury of the transplanted kidney. Transpl Proc. 2006;38:46–8.CrossRef Masztalerz M, Wlodarczyk Z, Czuczejko J, Slupski M, Kedziora J. Superoxide anion as a marker of ischemia-reperfusion injury of the transplanted kidney. Transpl Proc. 2006;38:46–8.CrossRef
5.
go back to reference Nath KA, Norby SM. Reactive oxygen species and acute renal failure. Am J Med. 2000;109:655–78.CrossRef Nath KA, Norby SM. Reactive oxygen species and acute renal failure. Am J Med. 2000;109:655–78.CrossRef
6.
go back to reference Das DK, Maulik N. Antioxidant effectiveness in ischemia reperfusion tissue injury. Methods Enzymol. 1994;233:601–10.PubMedCrossRef Das DK, Maulik N. Antioxidant effectiveness in ischemia reperfusion tissue injury. Methods Enzymol. 1994;233:601–10.PubMedCrossRef
7.
go back to reference Ikeda K, Negishi H, Yamori Y. Antioxidant nutrients and hypoxia/ischemia brain injury in rodents. Toxicology. 2003;189:55–61.PubMedCrossRef Ikeda K, Negishi H, Yamori Y. Antioxidant nutrients and hypoxia/ischemia brain injury in rodents. Toxicology. 2003;189:55–61.PubMedCrossRef
8.
go back to reference Rakotovao A, Berthonneche C, Guiraud A, de Lorgeril M, Salen P, de Leiris J, Boucher F. Ethanol, wine, and experimental cardioprotection in ischemia/reperfusion: role of the prooxidant/antioxidant balance. Antioxid Redox Signal. 2004;6:431–8.PubMedCrossRef Rakotovao A, Berthonneche C, Guiraud A, de Lorgeril M, Salen P, de Leiris J, Boucher F. Ethanol, wine, and experimental cardioprotection in ischemia/reperfusion: role of the prooxidant/antioxidant balance. Antioxid Redox Signal. 2004;6:431–8.PubMedCrossRef
9.
go back to reference Glantzounis GK, Salacinski HJ, Yang W, Davidson BR, Seifalian AM. The contemporary role of antioxidant therapy in attenuating liver ischemia-reperfusion injury: a review. Liver Transpl. 2005;11:1031–47.PubMedCrossRef Glantzounis GK, Salacinski HJ, Yang W, Davidson BR, Seifalian AM. The contemporary role of antioxidant therapy in attenuating liver ischemia-reperfusion injury: a review. Liver Transpl. 2005;11:1031–47.PubMedCrossRef
10.
go back to reference Kacmaz A, Polat A, User Y, Tilki M, Ozkan S, Sener G. Octreotide improves reperfusion-induced oxidative injury in acute abdominal hypertension in rats. J Gastrointest Surg. 2004;8:113–9.PubMedCrossRef Kacmaz A, Polat A, User Y, Tilki M, Ozkan S, Sener G. Octreotide improves reperfusion-induced oxidative injury in acute abdominal hypertension in rats. J Gastrointest Surg. 2004;8:113–9.PubMedCrossRef
11.
go back to reference Singh D, Chander V, Chopra K. Protective effect of catechin on ischemia-reperfusion-induced renal injury in rats. Pharmocal Rep. 2005;57:70–6. Singh D, Chander V, Chopra K. Protective effect of catechin on ischemia-reperfusion-induced renal injury in rats. Pharmocal Rep. 2005;57:70–6.
12.
go back to reference Benjamin B, Ebert L, Bunn HF. Regulation of erythropoietin gene. Blood. 1999;94:1864–77. Benjamin B, Ebert L, Bunn HF. Regulation of erythropoietin gene. Blood. 1999;94:1864–77.
13.
go back to reference Siren AL, Ehrenreich H. Erythropoietin: a novel concept for neuroprotection. Eur Arch Psychiatry Clin Neurosci. 2001;251:179–84.PubMedCrossRef Siren AL, Ehrenreich H. Erythropoietin: a novel concept for neuroprotection. Eur Arch Psychiatry Clin Neurosci. 2001;251:179–84.PubMedCrossRef
14.
15.
go back to reference Westenfelder C, Biddle DL, Baranowski RL. Human, rat and mouse kidney cells express functional erythropoietin receptors. Kidney Int. 1999;55:808–20.PubMedCrossRef Westenfelder C, Biddle DL, Baranowski RL. Human, rat and mouse kidney cells express functional erythropoietin receptors. Kidney Int. 1999;55:808–20.PubMedCrossRef
16.
go back to reference Calo LA, Bertipaglia L, Pagnin E. Antioxidants, carnitine and erythropoietin. G Ital Nefrol. 2006;34:47–50. Calo LA, Bertipaglia L, Pagnin E. Antioxidants, carnitine and erythropoietin. G Ital Nefrol. 2006;34:47–50.
17.
go back to reference Aluclu MU, Acar A, Guzel A, Bahceci S, Yaldiz M. Evaluation of erythropoietin effects on cerebral ischemia in rats. Neuro Endocrinol Lett. 2007;28:170–4.PubMed Aluclu MU, Acar A, Guzel A, Bahceci S, Yaldiz M. Evaluation of erythropoietin effects on cerebral ischemia in rats. Neuro Endocrinol Lett. 2007;28:170–4.PubMed
18.
go back to reference Lipsic E, Schoemaker RG, van der Meer P, Voors AA, van Veldhuisen DJ, van Gilst WH. Protective effects of erythropoietin in cardiac ischemia: from bench to bedside. J Am Coll Cardiol. 2006;48:2161–7.PubMedCrossRef Lipsic E, Schoemaker RG, van der Meer P, Voors AA, van Veldhuisen DJ, van Gilst WH. Protective effects of erythropoietin in cardiac ischemia: from bench to bedside. J Am Coll Cardiol. 2006;48:2161–7.PubMedCrossRef
19.
go back to reference Sepodes B, Maio R, Pinto R, Sharples E, Oliveira P, McDonald M, Yaqoob M, Thiemermann C, Mota-Filipe H. Recombinant human erythropoietin protects the liver from hepatic ischemia reperfusion injury in the rat. Transpl Int. 2006;19:919–26.PubMedCrossRef Sepodes B, Maio R, Pinto R, Sharples E, Oliveira P, McDonald M, Yaqoob M, Thiemermann C, Mota-Filipe H. Recombinant human erythropoietin protects the liver from hepatic ischemia reperfusion injury in the rat. Transpl Int. 2006;19:919–26.PubMedCrossRef
20.
go back to reference Wu H, Ren B, Zhu J, Dong G, Xu B, Wang C, Zheng X, Jing H. Pretreatment with recombined human erythropoietin attenuates ischemia-reperfusion-induced lung injury in rats. Eur J Cardiothorac Surg. 2006;29:902–7.PubMedCrossRef Wu H, Ren B, Zhu J, Dong G, Xu B, Wang C, Zheng X, Jing H. Pretreatment with recombined human erythropoietin attenuates ischemia-reperfusion-induced lung injury in rats. Eur J Cardiothorac Surg. 2006;29:902–7.PubMedCrossRef
21.
go back to reference Plotnikov EY, Chupyrkina AA, Jankauskas SS, Pevzner IB, Silachev DN, Skulachev VP, Zorov DB. Mechanisms of nephroprotective effect of mitochondria-targeted antioxidants under rhabdomyolysis and ischemia/reperfusion. Biochim Biophys Acta. 2011;1812:77–86.PubMedCrossRef Plotnikov EY, Chupyrkina AA, Jankauskas SS, Pevzner IB, Silachev DN, Skulachev VP, Zorov DB. Mechanisms of nephroprotective effect of mitochondria-targeted antioxidants under rhabdomyolysis and ischemia/reperfusion. Biochim Biophys Acta. 2011;1812:77–86.PubMedCrossRef
22.
go back to reference Poeggeler B, Saarela S, Reiter RJ, Tan DX, Chen LD, Manchester LC, Barlow-Warden LR. Melatonin: a highly potent endogenous radical scavenger and electron donor new aspects of the oxidation chemistry of this indole accessed in vitro. Ann NY Acad Sci. 1994;17:419–29. Poeggeler B, Saarela S, Reiter RJ, Tan DX, Chen LD, Manchester LC, Barlow-Warden LR. Melatonin: a highly potent endogenous radical scavenger and electron donor new aspects of the oxidation chemistry of this indole accessed in vitro. Ann NY Acad Sci. 1994;17:419–29.
23.
go back to reference Reiter RJ, Tan DX, Osuna C, Gitto E. Actions of melatonin in the reduction of oxidative stress: a review. J Biomed Sci. 2000;7:444–58.PubMedCrossRef Reiter RJ, Tan DX, Osuna C, Gitto E. Actions of melatonin in the reduction of oxidative stress: a review. J Biomed Sci. 2000;7:444–58.PubMedCrossRef
24.
go back to reference Reiter RJ, Tan DX, Pilar Terron M, Flores LJ, Czarnocki Z. Melatonin and its metabolites: new findings egarding their production and their radical scavenging actions. Acta Biochim Pol. 2007;54:1–9.PubMed Reiter RJ, Tan DX, Pilar Terron M, Flores LJ, Czarnocki Z. Melatonin and its metabolites: new findings egarding their production and their radical scavenging actions. Acta Biochim Pol. 2007;54:1–9.PubMed
25.
go back to reference Tan DX, Chen LD, Poeggeler B, Manchester LC, Reiter RJ. Melatonin: a potent endogenous hydroxyl radical scavenger. Endocr J. 1993;1:57–60. Tan DX, Chen LD, Poeggeler B, Manchester LC, Reiter RJ. Melatonin: a potent endogenous hydroxyl radical scavenger. Endocr J. 1993;1:57–60.
26.
go back to reference Carrillo-Vico A, Guerrero JM, Lardone PJ, Reiter RJ. A review of the multiple actions of melatonin on the immune system. Endocrine. 2005;27:189–200.PubMedCrossRef Carrillo-Vico A, Guerrero JM, Lardone PJ, Reiter RJ. A review of the multiple actions of melatonin on the immune system. Endocrine. 2005;27:189–200.PubMedCrossRef
27.
go back to reference Mayo JC, Sainz RM, Tan DX, Hardeland R, Leon J, Rodriguez C, Reiter RJ. Anti-inflammatory actions of melatonin and its metabolites, N1-acetyl-N2-formyl-5-methoxykynuramine (AFMK) and N1-acetyl-5-methoxykynuramine(AMK), in macrophages. J Neuroimmunol. 2005;165:139–49.PubMedCrossRef Mayo JC, Sainz RM, Tan DX, Hardeland R, Leon J, Rodriguez C, Reiter RJ. Anti-inflammatory actions of melatonin and its metabolites, N1-acetyl-N2-formyl-5-methoxykynuramine (AFMK) and N1-acetyl-5-methoxykynuramine(AMK), in macrophages. J Neuroimmunol. 2005;165:139–49.PubMedCrossRef
28.
go back to reference Reiter RJ, Tan DX, Maldonado MD. Melatonin as an antioxidant: physiology versus pharmacology. J Pineal Res. 2005;39:215–6.PubMedCrossRef Reiter RJ, Tan DX, Maldonado MD. Melatonin as an antioxidant: physiology versus pharmacology. J Pineal Res. 2005;39:215–6.PubMedCrossRef
29.
go back to reference Rodriguez C, Mayo JC, Sainz RM, Antolín I, Herrera F, Martín V, Reiter RJ. Regulation of antioxidant enzymes: a significant role for melatonin. J Pineal Res. 2004;36:1–9.PubMedCrossRef Rodriguez C, Mayo JC, Sainz RM, Antolín I, Herrera F, Martín V, Reiter RJ. Regulation of antioxidant enzymes: a significant role for melatonin. J Pineal Res. 2004;36:1–9.PubMedCrossRef
30.
go back to reference Maldonado MD, Murillo-Cabezas F, Terron MP, Flores LJ, Tan DX, Manchester LC, Reiter RJ. The potential of melatonin in reducing morbidity-mortality after craniocerebral trauma. J Pineal Res. 2007;42:1–11.PubMedCrossRef Maldonado MD, Murillo-Cabezas F, Terron MP, Flores LJ, Tan DX, Manchester LC, Reiter RJ. The potential of melatonin in reducing morbidity-mortality after craniocerebral trauma. J Pineal Res. 2007;42:1–11.PubMedCrossRef
31.
go back to reference Reiter RJ, Guerrero JM, Garcia JJ, Acuna-Castroviejo D. Reactive oxygen intermediates, molecular damage, and aging: relation to melatonin. Ann NY Acad Sci. 1998;854:410–24.PubMedCrossRef Reiter RJ, Guerrero JM, Garcia JJ, Acuna-Castroviejo D. Reactive oxygen intermediates, molecular damage, and aging: relation to melatonin. Ann NY Acad Sci. 1998;854:410–24.PubMedCrossRef
32.
go back to reference Kurcer Z, Oguz E, Ozbilge H, Baba F, Aksoy N, Celik H, Cakir H, Gezen MR. Melatonin protects from ischemia/reperfusion-induced renal injury in rats: this effect is not mediated by proinflammatory cytokines. J Pineal Res. 2007;43(2):172–8.PubMedCrossRef Kurcer Z, Oguz E, Ozbilge H, Baba F, Aksoy N, Celik H, Cakir H, Gezen MR. Melatonin protects from ischemia/reperfusion-induced renal injury in rats: this effect is not mediated by proinflammatory cytokines. J Pineal Res. 2007;43(2):172–8.PubMedCrossRef
35.
go back to reference Paglia DE, Valentine WN. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med. 1967;70:158–69.PubMed Paglia DE, Valentine WN. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med. 1967;70:158–69.PubMed
36.
go back to reference Ey Sšzmen, Sšzmen B, Delen Y, Onat T. Catalase/superoxide dismutase (SOD) and catalase/paraoxanase (PON) ratio may implicate poor glycemic control. Arch Med Res. 2001;32:283–7.CrossRef Ey Sšzmen, Sšzmen B, Delen Y, Onat T. Catalase/superoxide dismutase (SOD) and catalase/paraoxanase (PON) ratio may implicate poor glycemic control. Arch Med Res. 2001;32:283–7.CrossRef
37.
go back to reference Miller NJ, Rice-Evans C, Davies MJ, Gopinathan V, Milner A. A novel method for measuring antioxidant capacity and its application for monitoring the antioxidant status in premature neonates. Clin Sci. 1993;84:407–12.PubMed Miller NJ, Rice-Evans C, Davies MJ, Gopinathan V, Milner A. A novel method for measuring antioxidant capacity and its application for monitoring the antioxidant status in premature neonates. Clin Sci. 1993;84:407–12.PubMed
38.
go back to reference Kiris I, Kapan S, Kilbas A, Yilmaz N, Altuntaş I, Karahan N, Okutan H. The protective effect of erythropoietin on renal injury induced by abdominal aortic-ischemia-reperfusion in rats. J Surg Res. 2008;149:206–13.PubMedCrossRef Kiris I, Kapan S, Kilbas A, Yilmaz N, Altuntaş I, Karahan N, Okutan H. The protective effect of erythropoietin on renal injury induced by abdominal aortic-ischemia-reperfusion in rats. J Surg Res. 2008;149:206–13.PubMedCrossRef
39.
go back to reference Carden DL, Granger DN. Pathophysiology of ischemia reperfusion injury. J Pathol. 2000;190:255–66.PubMedCrossRef Carden DL, Granger DN. Pathophysiology of ischemia reperfusion injury. J Pathol. 2000;190:255–66.PubMedCrossRef
40.
go back to reference Noiri E, Nakao A, Uchida K, Tsukahara H, Ohno M, Fujita T, Brodsky S, Goligorsky MS. Oxidative and nitrosative stress in acute renal ischemia. Am J Physiol Renal Physiol. 2001;281:F948–57.PubMed Noiri E, Nakao A, Uchida K, Tsukahara H, Ohno M, Fujita T, Brodsky S, Goligorsky MS. Oxidative and nitrosative stress in acute renal ischemia. Am J Physiol Renal Physiol. 2001;281:F948–57.PubMed
41.
go back to reference Sekhon CS, Sekhon BK, Singh I, Orak JK, Singh AK. Attenuation of renal ischemia/reperfusion injury by a triple drug combination therapy. J Nephrol. 2003;16:63–74.PubMed Sekhon CS, Sekhon BK, Singh I, Orak JK, Singh AK. Attenuation of renal ischemia/reperfusion injury by a triple drug combination therapy. J Nephrol. 2003;16:63–74.PubMed
42.
go back to reference Kevin LG, Novalija E, Stowe DF. Reactive oxygen species as mediators of cardiac injury and protection: the relevance to anesthesia practice. Anesth Analg. 2005;101:1275–87.PubMedCrossRef Kevin LG, Novalija E, Stowe DF. Reactive oxygen species as mediators of cardiac injury and protection: the relevance to anesthesia practice. Anesth Analg. 2005;101:1275–87.PubMedCrossRef
43.
44.
go back to reference Hagiwara S, Koga H, Iwasaka H, Kudo K, Hasegawa A, Kusaka J, Yokoi I, Noguchi T. ETS-GS, a new antioxidant, ameliorates renal ischemia-reperfusion injury in a rodent model. J Surg Res. 2011;171:226–33.PubMedCrossRef Hagiwara S, Koga H, Iwasaka H, Kudo K, Hasegawa A, Kusaka J, Yokoi I, Noguchi T. ETS-GS, a new antioxidant, ameliorates renal ischemia-reperfusion injury in a rodent model. J Surg Res. 2011;171:226–33.PubMedCrossRef
45.
go back to reference Schoenberg MH, Beger HG. Reperfusion injury after intestinal ischemia. Crit Med Care. 1993;21:1376–86.CrossRef Schoenberg MH, Beger HG. Reperfusion injury after intestinal ischemia. Crit Med Care. 1993;21:1376–86.CrossRef
46.
go back to reference Mun KC, Lee HG, Lee TH, Kim YH, Kwak CS, Kim SP, Chang EJ, Park SB, Kim HC. Effect of modified polyhemoglobin on the ischemia/reperfusion injury in kidney. Transpl Proc. 2003;35:99–100.CrossRef Mun KC, Lee HG, Lee TH, Kim YH, Kwak CS, Kim SP, Chang EJ, Park SB, Kim HC. Effect of modified polyhemoglobin on the ischemia/reperfusion injury in kidney. Transpl Proc. 2003;35:99–100.CrossRef
47.
go back to reference Kiris I, Okutan H, Savas C, Yönden Z, Delibaş N. Deneysel aortic iskemi-reperfuzyon modelinde renal hasara gadolinium klorurun etkisi.Turkish. J Vasc Surg. 2005;14:13–8. Kiris I, Okutan H, Savas C, Yönden Z, Delibaş N. Deneysel aortic iskemi-reperfuzyon modelinde renal hasara gadolinium klorurun etkisi.Turkish. J Vasc Surg. 2005;14:13–8.
48.
go back to reference Chen CF, Hsueh CW, Tang TS, Wang D, Shen CY, Pei JS. Reperfusion liver injury induced superoxide dismutase and catalase expressions and the protective effects of N-acetyl cysteine. Transpl Proc. 2007;39:858–60.CrossRef Chen CF, Hsueh CW, Tang TS, Wang D, Shen CY, Pei JS. Reperfusion liver injury induced superoxide dismutase and catalase expressions and the protective effects of N-acetyl cysteine. Transpl Proc. 2007;39:858–60.CrossRef
49.
go back to reference Gulmen S, Kiris I, Narin C, Ceylan BG, Mermi B, Sutcu R, Meteoglu I. Tezosentan reduces the renal injury induced by abdominal aortic ischemia-reperfusion in rats. J Surg Res. 2009;157:e7–13.PubMedCrossRef Gulmen S, Kiris I, Narin C, Ceylan BG, Mermi B, Sutcu R, Meteoglu I. Tezosentan reduces the renal injury induced by abdominal aortic ischemia-reperfusion in rats. J Surg Res. 2009;157:e7–13.PubMedCrossRef
50.
51.
go back to reference Dimitrijevic ZM, Cvetkovic TP, Djordjevic VM, Pavlovic DD, Stefanovic NZ, Stojanovic IR, Paunovic GJ, Velickovic-Radovanovic RM. How the duration period of erythropoietin treatment influences the oxidative status of hemodialysis patients. Int J Med Sci. 2012;9(9):808–15.PubMedCentralPubMedCrossRef Dimitrijevic ZM, Cvetkovic TP, Djordjevic VM, Pavlovic DD, Stefanovic NZ, Stojanovic IR, Paunovic GJ, Velickovic-Radovanovic RM. How the duration period of erythropoietin treatment influences the oxidative status of hemodialysis patients. Int J Med Sci. 2012;9(9):808–15.PubMedCentralPubMedCrossRef
52.
go back to reference Ates E, Yalcin AU, Yılmaz S, Koken T, Tokyol C. Protective effect of erythropoietin on renal ischemia and reperfusion injury. ANZ J Surg. 2005;75:1100–5.PubMedCrossRef Ates E, Yalcin AU, Yılmaz S, Koken T, Tokyol C. Protective effect of erythropoietin on renal ischemia and reperfusion injury. ANZ J Surg. 2005;75:1100–5.PubMedCrossRef
53.
go back to reference Reiter RJ, Oh C-S, Fujimori O. Melatonin: its intracellular and genomic actions. Trends Endocrinol Metab. 1996;7:22–7.PubMedCrossRef Reiter RJ, Oh C-S, Fujimori O. Melatonin: its intracellular and genomic actions. Trends Endocrinol Metab. 1996;7:22–7.PubMedCrossRef
54.
go back to reference Paller MS. Pathophysiologic mechanisms of acute renal failure. In: Goldstein RS, editor. Mechanisms of injury in renal disease and toxicity. Michigan: Ann Arbor CRC Press; 1994. p. 3–13. Paller MS. Pathophysiologic mechanisms of acute renal failure. In: Goldstein RS, editor. Mechanisms of injury in renal disease and toxicity. Michigan: Ann Arbor CRC Press; 1994. p. 3–13.
55.
go back to reference Spandou E, Tsouchnikas I, Karkavelas G, Dounousi E, Simeonidou C, Guiba-Tziampiri O, Tsakiris D. Erythropoietin attenuates renal injury in experimental acute renal failure ischaemic/reperfusion model. Nephrol Dial Transpl. 2006;21:330–6.CrossRef Spandou E, Tsouchnikas I, Karkavelas G, Dounousi E, Simeonidou C, Guiba-Tziampiri O, Tsakiris D. Erythropoietin attenuates renal injury in experimental acute renal failure ischaemic/reperfusion model. Nephrol Dial Transpl. 2006;21:330–6.CrossRef
56.
go back to reference Quiroz Y, Ferrebuz A, Romero F, Vaziri ND, Rodriguez-Iturbe B. Melatonin ameliorates oxidative stress, inflammation, proteinuria, and progression of renal damage in rats with renal mass reduction. Am J Physiol Renal Physiol. 2008;294(2):F336–44.PubMedCrossRef Quiroz Y, Ferrebuz A, Romero F, Vaziri ND, Rodriguez-Iturbe B. Melatonin ameliorates oxidative stress, inflammation, proteinuria, and progression of renal damage in rats with renal mass reduction. Am J Physiol Renal Physiol. 2008;294(2):F336–44.PubMedCrossRef
57.
go back to reference Song Y, Chan CW, Brown GM, Pang SF, Silverman M. Studies of the renal action of melatonin: evidence that the effects are mediated by 37 kDa receptors of the Mel1a subtype localized primarily to the basolateral membrane of the proximal tubule. FASEB J. 1997;11(1):93–100.PubMed Song Y, Chan CW, Brown GM, Pang SF, Silverman M. Studies of the renal action of melatonin: evidence that the effects are mediated by 37 kDa receptors of the Mel1a subtype localized primarily to the basolateral membrane of the proximal tubule. FASEB J. 1997;11(1):93–100.PubMed
58.
go back to reference Singh I, Gulati S, Orak JK, Singh AK. Expression of antioxidant enzymes in rat kidney during ischemia-reperfusion injury. Mol Cell Biochem. 1993;125:97–104.PubMedCrossRef Singh I, Gulati S, Orak JK, Singh AK. Expression of antioxidant enzymes in rat kidney during ischemia-reperfusion injury. Mol Cell Biochem. 1993;125:97–104.PubMedCrossRef
59.
go back to reference Davies SJ, Reichardt-Pascal SY, Vaughan D, Russell GI. Differential effect of ischaemia-reperfusion injury on anti-oxidant enzyme activity in the rat kidney. Exp Nephrol. 1995;3:348–54.PubMed Davies SJ, Reichardt-Pascal SY, Vaughan D, Russell GI. Differential effect of ischaemia-reperfusion injury on anti-oxidant enzyme activity in the rat kidney. Exp Nephrol. 1995;3:348–54.PubMed
60.
go back to reference Conti M, Eschwege P, Ahmed M, Paradis V, Droupy S, Loric S, Bedossa P, Charpentier B, Legrand A, Benoit G. Antioxidant enzymatic activities and renal warm ischemia: correlation with the duration of ischemia. Transpl Proc. 2000;32:2740–1.CrossRef Conti M, Eschwege P, Ahmed M, Paradis V, Droupy S, Loric S, Bedossa P, Charpentier B, Legrand A, Benoit G. Antioxidant enzymatic activities and renal warm ischemia: correlation with the duration of ischemia. Transpl Proc. 2000;32:2740–1.CrossRef
61.
go back to reference Li Z, Nickkholgh A, Yi X, Bruns H, Gross ML, Hoffmann K, Mohr E, Zorn M, Büchler MW, Schemmer P. Melatonin protects kidney grafts from ischemia/reperfusion injury through inhibition of NF-kB and apoptosis after experimental kidney transplantation. J Pineal Res. 2009;46:365–72.PubMedCrossRef Li Z, Nickkholgh A, Yi X, Bruns H, Gross ML, Hoffmann K, Mohr E, Zorn M, Büchler MW, Schemmer P. Melatonin protects kidney grafts from ischemia/reperfusion injury through inhibition of NF-kB and apoptosis after experimental kidney transplantation. J Pineal Res. 2009;46:365–72.PubMedCrossRef
62.
go back to reference Sharples EJ, Patel N, Brown P, Stewart K, Mota-Philipe H, Sheaff M, Kieswich J, Allen D, Harwood S, Raftery M, Thiemermann C, Yaqoob MM. Erythropoietin protects he kidney against the injury and dysfunction caused by ischemia-reperfusion. J Am Soc Nephrol. 2004;15:2115–24.PubMedCrossRef Sharples EJ, Patel N, Brown P, Stewart K, Mota-Philipe H, Sheaff M, Kieswich J, Allen D, Harwood S, Raftery M, Thiemermann C, Yaqoob MM. Erythropoietin protects he kidney against the injury and dysfunction caused by ischemia-reperfusion. J Am Soc Nephrol. 2004;15:2115–24.PubMedCrossRef
63.
go back to reference Vesey DA, Cheung C, Pat B, Endre Z, Gobé G, Johnson DW. Erythropoietin protects against ischaemic acute renal injury. Nephrol Dial Transplant. 2004;19:348–55.PubMedCrossRef Vesey DA, Cheung C, Pat B, Endre Z, Gobé G, Johnson DW. Erythropoietin protects against ischaemic acute renal injury. Nephrol Dial Transplant. 2004;19:348–55.PubMedCrossRef
64.
go back to reference Sener G, Sehirli AO, Keyer-Uysal M, Arbak S, Ersoy Y, Yegen BC. The protective effect of melatonin on renal ischemia-reperfusion injury in the rat. J Pineal Res. 2002;32:120–6.PubMedCrossRef Sener G, Sehirli AO, Keyer-Uysal M, Arbak S, Ersoy Y, Yegen BC. The protective effect of melatonin on renal ischemia-reperfusion injury in the rat. J Pineal Res. 2002;32:120–6.PubMedCrossRef
Metadata
Title
Effect of a combined treatment with erythropoietin and melatonin on renal ischemia reperfusion injury in male rats
Authors
Nasser Ahmadiasl
Shokofeh Banaei
Alireza Alihemati
Behzad Baradaran
Ehsan Azimian
Publication date
01-12-2014
Publisher
Springer Japan
Published in
Clinical and Experimental Nephrology / Issue 6/2014
Print ISSN: 1342-1751
Electronic ISSN: 1437-7799
DOI
https://doi.org/10.1007/s10157-014-0937-6

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